Basidiomycete fungi are the major agents of decomposition and nutrient cycling in forest ecosystems. Different species and individuals encounter each other both within colonized organic substrata and in soil/leaf litter during outgrowth in search of new resources. They defend and obtain new territory by combative, antagonistic interactions. These interactions are, thus, crucial to fungal community development and functioning in dead organic matter. The overall outcomes are deadlock, where neither species gains headway, or replacement where one species wrests territory from the other, but sometimes partial replacement or mutual replacement. Outcomes vary depending on species, site of interaction (i.e. in soil or wood etc.), microclimate and relative size of mycelia and resources occupied etc. Outcome of interactions can be affected by microclimate and resource status amongst others. Recently we have shown that soil invertebrate grazing alters mycelial interactions, dramatically. With the complexity of multiple species and environmental conditions, many different antagonistic mechanisms operate. Responses to antagonists include rapid cell division and death, production of pigments, volatile (VOCs) and diffusible organic compounds, and other antimicrobial agents. We are trying to understand both how interspecific fungal interactions determine fungal community structure and development, and the underlying mechanisms of antagonism.Ultimately we want to know how wood decay communities function in natural ecosystems. We are investigating the physiological changes during interactions between species of decay fungi in wood representing the succession from primary coloniser to secondary and tertiary decomposers, under differing environmental conditions, using new post-genomic tools to allow us to get a complete picture of the genes that are switched on and off during interactions.

Many invertebrates are attracted to fungal mycelia and fruit bodies, upon which they may graze and in which they may breed. The mycelial morphology and physiological/biochemical functioning of saprotrophic soil basidiomycetes can alter dramatically in the presence of nematodes, collembolan, woodlice and other invertebrates. Detailed studies of the effects of soil invertebrates on saprotrophic cord-forming fungi have revealed dramatic changes to mycelial patterns in laboratory soil microcosm studies. These changes depend both on invertebrate grazer species and on fungal species.

Mycelial cord systems of Phanerochaete velutina ramifying across the floor of a mixed deciduous woodland.

In turn, soil fungi influence soil invertebrate populations. In our most recent studies we have come closer to the real world by using soil mesocosms and also by manipulating presence/absence of cord-forming fungi and the size of woodlice populations in soil in deciduous woodland. Metagenomic sequencing, enzyme assays, fungal biomass assessment and invertebrate counts are revealing effects of invertebrate grazing on soil microbial community structure and functioning. There are both bottom up and top down effects. A recent paper on this by A’Bear et al. (2013) Bottom-up determination of soil collembola diversity and population dynamics in response to interactive climatic factors., Oecologia 173, 1083-1087. (DOI: 10.3410/f.718002562.793489295), was selected for F1000Prime, and recommended as being of special significance in its field.

Ecology of endangered woodland basidiomycetes

Funding bodies: Natural England

External collaborators: A. Martyn Ainsworth (Kew Gardens)

BIOSI collaborator: Hilary J. Rogers

Post-docs: David Parfitt

Hericium coralloides in snow. Copyright Martyn Ainsworth.

We are seeking to reveal whether a set of wood decomposer and ectomycorrhizal species, thought to be rare based on paucity of fruiting records, are actually rare and endangered, and if so then why? Fungi in the genus Hericium (hedgehog fungi) are decomposers of wood and other plant litter. H. erinaceum is a UK BAP priority species, and H. coralloides appears even rarer, H. cirrhatum is also uncommon. Concentrating on these species, we have obtained probably the most in depth autecological knowledge of any putatively rare fungal species. In a similar project with Piptoporus quercinus – the rare oak polypore, we have found that populations appear to be inbred, sexual spores rarely germinate, but thick-walled asexual spores allow survival under adverse microclimate. Having developed specific PCR primers for these BAP fungi we are now in a position to discover whether they are really rare or whether they just produce visible fruit bodies infrequently.

Some mycorrhizal basidiomycetes are also rare or endangered, particularly stipitate hydnoids and some boletes. These fungi are not currently culturable and fruit bodies of some species are often hard to distinguish from those of others. Before we can investigate their ecology we need to be able to identify them (both as fruit bodies and as mycelia). Currently we are using molecular approaches to reveal cryptic taxa, and to construct species specific PCR primers.

Foraging patterns, and architecture of mycelia systems in soil

Funding bodies: NERC

External collaborators: Mark D. Fricker (University of Oxford)

Mycelial cord systems of Phanerochaete velutina ramifying across the floor of a mixed deciduous woodland.

Wood-decaying basidiomycete fungi are the major agents of decomposition in forests and hence crucial to nutrient cycling. On the forest floor, decay fungi that produce ‘root-like’ linear organs - termed cords, exhibit remarkable patterns of biomass and nutrient reallocation on locating new resources. They also deploy biomass differently and operate different search patterns depending on species, microclimatic regime, nutrient status of the system and surrounding soil.

We are seeking to understand how the balance between the metabolic requirements of the fungus and the need to conserve nutrients determines the patterns of mycelial system development, and the rates, routes and direction of nutrient (N, P, K) movement within mycelial systems, particularly the common woodland fungi Phanerochaete velutina, Phallus impudicus (stinkhorn), Hypholoma fasciculare (sulphur tuft) and Resinicium bicolor.

Image analysis and fractal geometry has revealed polarised growth of mycelial cord systems of P. velutina towards newly encountered resources even when these are relatively small. N, P, K status of both soil and the resource from which the fungus is growing critically affects foraging behaviour and fractal dimension, and the response of mycelia to newly encountered resources. Phosphorus is moved from existing to newly-encountered resources. However, local supply of phosphorus from soil adjacent to the new resource is up to 100 times greater than that moved in from elsewhere.

Cords in tropical rainforest (photographed by Rory Bolton).

We are also seeking to understand the enzymology associated with obtaining nutrients from dead organic matter in nature. We have just begun to investigate spatial and temporal variation in enzyme activity in wood and soil associated with different regions of mycelium, with Peter Baldrian.

The complex mycelial networks that form in soil are constantly being remodelled in response to nutrient discovery and demand, changes in microclimate and destructive disturbance, e.g. by invertebrate grazers. We are currently investigating, mathematically, the architecture of networks, routes between different regions, resilience to damage, etc. using graph/network theory, in collaboration with Mark Fricker at Oxford.

Wood decomposition and fungal community development begins while branches are still in the canopy and trunks still standing. In at least eight angiosperm tree species, extensive (several to many metres) decay columns develop in less than one growing season. These decay columns are much longer than could be achieved by a fungus extending by mycelial growth from a single inoculum point. Instead, fungal propagules are extensively but sparsely distributed throughout the sap stream, but do not develop overtly because of the high water content. Thus, if the high water content (low O2, low nutrient availability) of functional sapwood is removed then mycelia will develop from these propagules, will quickly meet and if they are the same genotype they will fuse and act as a single individual. This has been shown to be the case in all broadleaved trees that we have tested, though with some species genetic differences in mycelia resulted in long decay columns containing several or sometimes many different fungal individuals.

Many questions remain, and to attempt to answer these we need sensitive techniques. Thus, we are using PCR-based approaches and 454 sequencing to begin to test the following hypotheses, which is essential to understand fully the early stages of tree death and wood decay in the natural environment:

Being ubiquitous, bacteria must frequently interact with fungal mycelia in nature, yet hitherto this has received very little attention. We have recently shown that saprotrophic mycelial cords growing in woodlands have a variety of bacteria closely associated with them, including members of the Burkholderiaceae. Laboratory soil microcosm studies have revealed that fungal mycelia have species specific effects on the adhering microbial community, and also that bacteria are rapidly suppressed during fungal colonization of wood.

Although bacteria are thought to have little direct effect on wood decay, they do interact with wood decay fungi and may make important contributions to the process in a range of different ways. Bacteria compete for the fungal-derived products of wood breakdown, and fungi have evolved mechanisms inhibitory to bacterial activity. A preliminary study indicates specific associations between the fungus colonizing wood and bacterial community diversity and abundance. The aim of ongoing work is to investigate, experimentally in the laboratory and field, the effects of different wood decay fungal species and stage of wood decomposition on bacterial community structure, activities and interactions.

Fungi provide vital ecosystem services through decomposition, nutrient cycling and soil aggregation, and are an important during consideration of ecosystem responses to global change. We have analysed data sets from the UK, Norway, Austria and Switzerland. From information we have revealed that fruiting phenology is changing in many European countries: on average, the fruiting season is extending, though for some species it is contracting; different species and ecological groups behave differently; time of fruiting depends on geographical location; some fungi now fruit early in the year as well as in autumn, and spring fruiting is getting earlier; some fungi appear to be changing hosts; the amount, duration and frequency of fruiting are influenced by numerous environmental factors. These changes are not only important in terms of extending the duration of production of fungal sexual spores, but more significantly fungi are now active over much longer periods, hence effecting decomposition.

We are now extending our analyses to: cover more European countries; determine whether detailed local data sets provide similar results to more diffuse national datasets; look more closely at different ecological groups of fungi; determine whether ‘host preferences’ have changed; determine whether there are changes in patterns of fruiting of fungi whose ecology is closely linked, e.g. host/parasite and predecessor/successors in community development.